The latest shallow-sea isocrinids from the Miocene of Paratethys and implications to the Mesozoic marine revolution

The predation-driven Mesozoic marine revolution (MMR) is believed to have induced a dramatic change in the bathymetric distribution of many shallow marine invertebrates since the late Mesozoic. For instance, stalked crinoids – isocrinids (Isocrinida) have undergone a striking decline in shallow-sea environments and today they are restricted to deep-sea settings (below 100 m depth). However, the timing and synchronicity of this shift are a matter of debate. A delayed onset of MMR and/or shifts to a retrograde, low-predation community structure during the Paleogene in the Southern Ocean were invoked. In particular, recent data from the Southern Hemisphere suggest that the environmental restriction of isocrinids to the deep-sea settings may have occurred at the end of the Eocene around Antarctica and Australia, and later in the early Miocene in New Zealand. Here, we report the anomalous occurrence of the isocrinids in shallow nearshore marine facies from the middle Miocene of Poland (Northern Hemisphere, Central Paratethys). Thus, globally, this is the youngest record of shallow-sea stalked crinoids. This finding suggests that some relict stalked crinoids may have been able to live in the shallow-water environments by the middle Miocene, and further confirms that the depth restriction of isocrinids to offshore environments was not synchronous on a global scale.

the Cenozoic occurrences of isocrinids from the Southern Hemisphere implies a continuous record of shallow marine isocrinids from the Cretaceous to the late Eocene, rather than temporal reversions 14 , suggesting that the timing of the onshore-offshore shift was not synchronous globally.
In this paper, we describe isocrinid ossicles from the middle Miocene shallow marine facies exposed in two localities in Poland.These findings not only represent the youngest global fossil record of shallow-sea isocrinids, but also support the view that occasionally, some stalked crinoids might have remained in the onshore environments long time after the initiation of the Mesozoic marine revolution.

Geological settings and stratigraphy
Field works aimed at collecting crinoid material were conducted in two localities in the southern Poland (Fig. 2), namely Gołuchów and Zygmuntów (near Książ Wielki).Gołuchów is located on the southern edge of the Holy Cross Mountains, approximately 30 km south of Kielce city and approximately 20 km east of Jędrzejów city.The outcrop is located in a disused quarry (coordinates: 50.622703N, 20.615972 E).Zygmuntów profile (near Książ Wielki) is located approximately 40 km southwest of Gołuchów and approximately 30 km south of Jędrzejów city.Herein, as a result of the construction of the S7 Cracow-Kielce expressway, Miocene sediments are exposed (coordinates: 50.26339N, 20.11198 E).
Our analyses of thin sections (Fig. 5a-c) taken from these rock levels suggest the presence of two facies types: (i) sandy limestone (FT 1-facies type 1) with numerous bioclasts (Fig. 5b,c) and (ii) sand and/or poorly lithified (sporadically marly) sandstone with numerous bioclasts (FT 2-facies type 2) (Fig. 5a).Numerous quartz grains and exclusively Miocene bioclasts embedded in the carbonate matrix are observed herein.FT 1 facies type is mostly represented by sandy limestone (rudstone-floatstone), within each numerous bored fragments of algal colony are present (Fig. 5b,c).Among bioclasts, abundant and well-preserved small and large benthic foraminifers (Amphistegina sp. and Heterostegina costata), molluscs, bryozoans and echinoderms were observed.The matrix is mostly composed of carbonates though small quartz grains are also observed.In the FT 2 sharp-edged quartz grains with a diameter of up to 1 mm, most often ~ 0.5 mm (Fig. 5a) are abundant.Glauconite grains are also common in these sediments.Among the bioclasts, Badenian small and large benthic foraminifers and polychaetes (Fig. 5a) were observed.Calcareous clasts up to 3 mm thick were also observed, in which fragments of red-algae and micritic sediments with small quartz grains resembling FT 1 can be distinguished.

Zygmuntów (near Książ Wielki)
In the newely exposed outcrop, sands with gravels embedded with two layers of clays, each with a thickness of about 0.6 m, and three layers of limestones, each 0.4 m thick, are present.Herein, within the lenses of sands and gravels, abundant benthic invertebrate fossils and fish teeth can be found.Crinoids were recorded in marly sands of the middle part of the section.Grill 56 and Studencka 55 based on characteristic bivalve assemblage suggested that these sediments belong to the Lagenidae Zone (early Badenian).
Our analyses of thin sections indicated that the bioclastic-reach sand and/or poorly lithified sandstone facies have limy matrix (Fig. 5d).Quartz grains typically have diameters of ~ 0.5 mm.Smaller grains are sharp-edged (Fig. 5e,f).Glauconite grains are also noted.Among numerous, exclusively Miocene bioclasts, we observed thick-shelled bivalves, bryozoans, serpulids, echinoids and fragments algal colonies (Fig. 5d-f).Abundant and well-preserved benthic foraminifers of various size (such as Amphistegina sp.) (Fig. 2f) are the most characteristic.Overall, this facies is similar to FT 1 observed in Gołuchów.

Palaeoenvironmental interpretation
Facies and microfacies (Figs. 4, 5) recorded in both localities can be ascribed to the so-called Heterostegina Sands.Facies type 2 belongs to algal-amphisteginid/heterosteginid facies 44 with numerous bryozoans and large benthic foraminifers.In general, these facies have been developed in near-shore shallow marine environment of moderate energy, that was occasionally subjected to storms, which resulted in faunal accumulations with coquina lags 41,46 .Mass occurance of well-preserved large foraminifers (Amphistegina and Heterostegina) are typical for shallow marine early Badenian Paratethys deposits.It is noteworthy that Recent representatives of Amphistegina prefer shallow-waters at a depth below 20 m 57 .No linear current sedimentary structures were observed, which is indicative of higher turbulance during storms.Previous studies based on analyses of the shallow-water fauna determined the palaeodepth of these sedimentary environment to be several to several dozen meters 36,38,39,42,46 .

Fish fossil assemblage
Apart from collected crinoid fossils, a number of fish teeth were recorded (they will be described in a separate paper elsewhere).In the Gołuchów quarry, quite numerous fish teeth were recorded, most of which belong to teleost fish (above 70% collected specimens).All of them belong to the family Sparidae (stratigraphic range No fish teeth from Mesozoic taxa were found at both sites.The stratigraphic ranges of all elasmobranch genera and teleost Sparidae are Cenozoic.Sparid fishes, whose teeth are present in Gołuchów are typically reef-associated forms and prefer warm and shallow water environments 63 .Sparid teeth are adapted to a durophagous diet and indicate feeding on shelled invertebrate fauna 58,60,63 .

Crinoid description
In both localities fragments of stems and isolated brachial of isocrinids were recorded (Fig. 6).Their detailed description is given below.Systematic description and terminology follows Hess and Messing 64 .Lumen is small and circular.Cirrus scars of nodal columnals are of similar diameter, with a width ranging from 33 to 46% of the nodal diameter.Cirrus scar height ranges from 72 to 87% of nodal height.They are oval and may be proximally short.Secundibrachial is muscular and rounded aborally.Pinnule socket is visible.Cirrus is oval and its latera is smooth.

Discussion
The material described herein is strikingly similar to those described from the Miocene of France and ascribed to metacrinid crinoids 68 .Among the subfamily Metacrininae, three genera (Metacrinus, Eometacrinus, Saracrinus) are known according to Hess and Messing 64 , but Améziane et al. 69 distinguished two genera (Metacrinus, Saracrinus) within this subfamily.Although Saracrinus is closely related to Metacrinus, Hess and Messing 64 based on opinions of Meyer and Oji 10 , Ameziane 70 and Roux et al. 71 decided to separate it from Metacrinus.Typical Saracrinus has 4 primibrachials, among which primibrachials 1 and 2 are united by cryptosyzygy.Similarly in the case of Metacrinus, cryptosyzygy occurs between primibrachials 1 and 2. In the case of species with 7 primibrachials, cryptosyzygy also occurs between primibrachials 4 and 5 or 5 and 6.In the case of secundibrachials cryptosyzygy occur between secundibrachials 2 and 3 or 3 and 4 and also in more distal parts of arms.Other articulations in brachials are muscular.In the case of Eometacrinus, 5 primibrachials are known and synarthry is known between primibrachials 1 and 2, and cryptosyzygy between primibrachials 4 and 5.All of the above indicate that without an access to more complete (articulated) arms of Metacrininae, it is not possible to classify isolated metacrinitid stem material at the genus level.This led to the inclusion of the current material in Metacrininae.

Discussion
Discovery of isocrinid crinoids from the shallow marine facies of the middle Miocene age in the southern Poland (Northern Hemisphere, Central Paratethys) has a number of palaeoecologic implications.Although, the presence of isocrinid columnals from this region (Książ Wielki) has been already noted in 1934 by Krach 79 , they were never described nor illustrated, and the scientific value of their occurrences was not appreciated.Subsequently, for a long time the outcrop has been overgrown and was not assessable to palaeontological investigations.However, recent roadworks, which enabled us to collect new samples containing isocrinid columnals, allowed us to thoroughly describe these important fossils.
Although our material is mostly disarticulated (Fig. 6), and represented predominantly by stem fragments, its morphologic (resemblance to other well known Miocene isocrinid taxa) and taphonomic features (some of the material represented by articulated non-abraded pluricolumnals showing ornamentation and delicate stereom microstructure), combined with the sedimentologic and palaeogeographic context (restricted nearshore bay www.nature.com/scientificreports/situated far away from the deeper slopes; see Fig. 2) suggest that these crinoids were paraautochthonous, i.e. they were not subject to significant transport and/or redeposition before final burial.Indeed, in-situ observations and tumbling experiments on Recent crinoids demonstrated that taphonomic features are a useful proxy in assessing autochthonous and allochthonous ossicles 80,81 .Those, which are subject to significant transport typically reveal altered (thinned or rounded) shape and broken stereom trabeculae with numerous shallow abrasion-induced grooves (wear scars).At least some of the material, especially from the Zygmuntów locality, does not reveal any of these features.Although the ossicles from Gołuchów, are not so well preserved -their disarticulation gradient is higher and some of them are slightly bioeroded/abraded -such features are typical in such high energy environment 4,82 .Finally, no evidence of post-diagenetic breakage on cleavage planes, which are indicative of reworking and redeposition from older rocks, were noted.Overall, these data suggest that some relic isocrinid fauna might have been able to live in shallow marine environments by the middle Miocene.These findings expand the number of isocrinid occurrences in the Cenozoic shallow marine facies.Importantly, our compilation and critical evaluation of published data (Fig. 1) on the Cenozoic shallow marine isocrinids, suggest that isocrinids from Poland, were actually the latest stalked crinoids which were able to live in the nearshore environment.This is quite surprising given the fact that in such environment, a variety of predators are common.Indeed, from both localities numerous teeth of fish predators (see above) and cidaroid echinoids were recorded [represented by common, shallow water, species Eucidaris zeamays 83 ].One may speculate that these crinoids might have not been a preferential prey for some of these predators at that time -today, at least some representatives of fish groups recorded in our localities (Sparidae) are known to prey upon crinoids 84 .One the other hand, fossil isocrinids, like their Recent descendants, are known to possess a number of anti-predatory adaptations (regeneration, autotomy and crawling abilities, among the others) [85][86][87][88] , which, to some extent, might help them survive in such an environment.
Notwithstanding, the results presented here suggest that the disappearance of isocrinids from shallow marine environments was asynchronous on a global scale.Not only in the Gondwana Realm they remained in shallow water long after the initiation of the Mesozoic marine revolution, but in Euramerica, some relic populations of isocrinid fauna might have been also able to inhabit such environments.

Materials and methods
Field works have been carried out in 2021 in Zygmuntów, and in 2023 in Gołuchów.Fossils, in particular crinoids, but also fish teeth, were initially searched in the field.At this stage, few of them have been collected.Additionally, bulk samples weighing 30 to 40 kg were taken from each lithological levels.In Gołuchów these were: red-algal sandy limestones with pebbles and fine-detrital sands or weakly compact calcareous and marly sandstones representing Heterostegina Sands, whereas in Zygmuntów, sands with gravel, clays and limestones were taken.Further work was carried out in the Palaeontological Laboratory of the Institute of Earth Sciences of the University of Silesia in Katowice.The marly samples were washed only with a stream of hot water and sieved through sieves with mesh diameters of 1.00 mm and 0.315 mm.Limestone samples were boiled in a Glauberian salt solution; after cooling, they were frozen.This process was repeated twice.The macerated rock was washed with hot water, sieved through sieves and dried at 180 °C.The obtained residue was examined for the presence of fauna using an Olympus SZX7-TR30 binocular.Crinoids were documented only in finely grained marly sands.